/. Emhryol. e.xp. Morph. Vol. 29, 2, pp. 431-437, 1973
43[
Printed in Great Britain
Appearance of antler pedicles in early
foetal life in red deer
By G. A. LINCOLN 1
From the Unit of Reproductive Biology, University of Liverpool
SUMMARY
The primordial antler pedicles of red deer show a transitory enlargement in early foetal
life in the male while no similar change occurs in the female. Observations on the growth
rate of the reproductive tract, pituitary and adrenal glands and the content of testosterone
in the gonads, indicate that the precocious development of the pedicles occurs during a
phase of increased testicular activity and probably reflects a surge in testosterone secretion
following sexual differentation.
INTRODUCTION
It is possible to sex a red deer foetus (Cervus elaphus) at an early age by close
inspection of the animal's forehead. In the male foetus a pair of conspicuous
swellings develop on the skull which are not found in the female. These structures represent the primordial antler pedicles, and following this early development they become inconspicuous until puberty when they resume growth and
give rise to the antlers.
It is well established that the development of antler pedicles in deer at puberty
is stimulated by the secretion of testosterone by the testis (Wislocki, Aub &
Waldo, 1947). The question arises as to whether the precocious development of
the antler pedicles in the foetus is also the result of increased testosterone secretion. It has been established in a number of other mammals that the testis is
active in early foetal life and is responsible for the differentation of the male
reproductive tract as well as influencing the form of the external genitalia (Burns,
1961). The present study attempts to find an explanation for the early growth of
the antler pedicles in red deer by comparing the development of the reproductive
system of the male foetus with that of the female.
MATERIALS AND METHODS
Ninety-six red deer foetuses weighing between 0-5 g and 525 g were collected
between 1968 and 1971 from hinds shot by Nature Conservancy stalkers on
estates in Scotland. They were stored in 10 % formalin and later sexed and
1
Author's address: Unit of Reproductive Biology, University of Liverpool, Life Sciences
Building, P.O. Box 147, Liverpool L69 3BX, U.K.
28-2
432
G. A. LINCOLN
weighed. The gonads, accessory glands, pituitary and adrenal glands were
removed under a dissecting microscope and weighed. The ano-genital distance,
neck girth and the appearance of the pedicles was also recorded. When the
foetuses were too small to be sexed on morphological grounds only the gonads
were weighed.
For simplification the animals of approximately the same size were grouped
together and the organ weights expressed as a mean for the group. Testosterone
was extracted from pooled samples of gonads from each group by the method
of Mann, Rowson, Short & Skinner (1967), purified by thin layer chromatography on Silica gel/CT (Reeve Angel Scientific), and measured by radio
immuno-assay using anti-sera raised to a testosterone conjugate (P. Rowe,
unpublished, Unit of Reproductive Biology, University of Liverpool). The
maximum sensitivity of the method was 50 pg of testosterone per animal. The
age of the foetuses was estimated from a regression line relating the cube root
of body weight to gestational age (Mitchell & Lincoln, in preparation) using a
mean gestation length for red deer of 233 days.
RESULTS
(a) Growth of the pituitary and adrenal glands. The weight of the pituitary
and adrenal glands increased steadily in relation to gestational age from 50 to
120 days (1 g to 600 g foetal weight) and there was no sex difference in the weight
of the glands at any stage (Fig. 1).
(b) Growth and testosterone content of the gonads. At 38-40 days of age
(0-5 gwt) the gonads were elongated bodies lying along the medio-ventral
surface of the enlarged mesonephric kidney and morphological separation of
the sexes was impossible at this stage. This distinction became possible by the
42nd day (1-5 g wt) when the testes became larger, rounder and firmer than the
ovaries.
From 45 to 95 days of gestational age the gonads of both sexes continued
growing rapidly with the testes remaining larger than the ovaries until about the
87th day (Fig. 6a). Over this period the gonads of both sexes moved slightly
posteriorly as the mesonephric kidney regressed and was replaced anteriorly
by the functional kidney of the adult. The testes reached a peak in weight in
foetuses of about 80 days of age (80 g wt) before becoming slightly reduced in
size during the period that they migrated from the posterior border of the kidney
to the neck of the inguinal canal (Figs. 4 and 5). In the females the ovaries retained
their abdominal position and reached maximum weight about 16 days after
the initial peak found in the growth of the testes (Fig. 6a). After this period of
growth the ovaries underwent rapid involution and at 100 days of foetal age
weighed less than half that of the testes at a similar stage.
Testosterone was not detected in pooled samples of gonads from foetuses
before 55 days of gestation, although it was possible to sex the animals at this
433
Foetal antlers
25 t—
10
20
l
40
50
60
640
40
80
160
Weight of embryo (g)
I
i
i
70
80
90
Davs of gestation
100
110
I I
120
Fig. 1. Weight of pituitary and adrenal glands from male ( # ) and female ( • ) red
deer foetuses related to body weight and gestational age. Each point shows the mean
and S.D. for groups of between five and eight animals.
stage. The hormone was detected in pooled samples of testes from animals of
55 to 65 days of age (10-30 g wt) and in all groups until 105 days. Testes from
animals between 105 and 120 days of age contained no detectable testosterone
as did extracts of ovaries at all stages (Fig. 6c).
(c) Growth of the external genitalia, accessory glands and secondary sexual
characters. While it was possible to determine the sex of a foetus on the appearance of the gonads at 42 days of gestational age (1-5 gwt) it was not until
about 7 days later (4-5 g wt) that sex differences were clearly visible in the form
of the external genitalia. After 50 days of age the male foetuses showed a rapid
increase in the ano-genital distance compared with the females (Fig. 6 b) and
434
G. A. L I N C O L N
Fig. 2. Male red deer foetus of about 97 days of age (204 g wt) showing conspicuous
antler pedicles on the forehead (indicated), and expanded neck girth, x 1-5.
Fig. 3. Female red deer foetus of about 94 days of age (170 g wt) for comparison with
Fig. 2. xl-5.
Fig. 4. Male red deer foetus of about 63 days of age (15 g wt) dissected to show
the reproductive tract about 3 weeks after sex differentation. Externally the scrotum
is just visible, the ano-genital distance is 17 mm, and the antler pedicles are just
apparent on the forehead, a, adrenal; b, metanephric kidney; c, mesonephric kidney;
d, testis; e, penis. x2.
Fig. 5. Male red deer foetus of about 88 days of age (121 g wt) showing the testes
during their descent towards the inguinal canal. At this stage the antler pedicles are
most conspicuous, x 1.
435
Foetal antlers
80
60
•5 40
20
O, x)
50
— E 40
S,
c
o ^ ' 30
CO u
c
6 ca 20
<c ."2
T3
10
0
o
O
Enlargement of antler pedicles
Enlargement of clitoris
i
10
40
50
20
60
I
i
320
40
80
160
Weight of embryo
70
80
90
Days of gestation
100
640
110
120
Fig. 6 {a). Weight of testes ( • ) , ovaries ( • ) and seminal vesicles (O) of red deer
foetuses related to gestational age. Mean value and S.D. for groups of animals are
shown.
(/>) Ano-genital distance of male ( • ) and female ( • ) foetuses related to age.
(c) Testosterone content of testes ( • ) and ovaries ( • ) related to age. Mean value
for groups of animals is shown.
(d) Period of enlargement of the antler pedicles in the male, and the clitoris in
the female; the double hatched area indicates when the organs were particularly
conspicuous.
436
G. A. LINCOLN
the penis assumed a more ventral position. The scrotum was apparent by 60 days
(15 g wt) and the seminal vesicles were identifiable by 70 days (40 g wt, Fig. 6a).
The antler pedicles first became apparent in male foetuses at about 60 days
of age (15 g wt) and from 75 to 100 days (60 g to 240 g wt) they were particularly
conspicuous (Figs. 2 and 3). Later they became less obvious apparently due to
differential growth of the surrounding tissue (Fig. 6d). The female foetuses often
showed opaque, slightly raised areas in the position of the antler pedicle but
these did not expand as in the male. In addition to this difference in the development of the antler pedicles, there was also a sex difference in the growth of the
neck musculature in early foetal life. In the male foetuses the neck girth increased
markedly over that found in the female, and this difference was most apparent
from 70 to 100 days of age. The mean neck girth of male foetuses at 62, 82 and
100 days of age was 36 mm, 53 mm and 97 mm respectively, while the corresponding measurements for the female foetuses were 35 mm, 46 mm and 93 mm
(Figs. 2 and 3).
While the female foetuses showed no changes in the antler pedicles and neck
musculature comparable to that of the male it was interesting that over the same
period they showed very pronounced hypertrophy of the clitoris. At about 70
days of age (40 g wt) the clitoris began to enlarge and between about 80 and
90 days of age (80 g to 150 g wt) it was most conspicuous (Fig. 6d).
DISCUSSION
During foetal development the gonads of red deer undergo a period of rapid
growth initiated prior to sex differentiation at 42 days of age and continuing
until about mid-gestation. In the male testosterone is present in the testes at
an early age, and it seems probable that the hormone is responsible for the
masculinizing changes which occur in the reproductive tract following sex differentiation. In addition, it is likely that the hypertrophy of the antler pedicles and
the expansion of the neck musculature of the male foetuses which occurs
between 50 and 100 days is also the direct result of a surge in testosterone
secretion which accompanies the period of increased testis activity. In adult life
both the antler pedicle and the neck musculature represent secondary sexual
characters which develop in response to testosterone (Lincoln, 1971), and the
present observations indicate that this androgen sensitivity" acquired in early
foetal life. Sex differences in the neck musculature of foetuses have also been
noted in the wapiti, Cervus canadensis (Retfalvi, 1969).
While both the foetal testis and ovary show a period of activity or growth
during the first half of gestation in the red deer, it is striking that testosterone
disappears from the testis, and the ovary becomes involuted after about the
110th day. This is of interest for it may indicate the development of a functional
negative feedback system from gonad to hypothalamus soon after the sex
differentiation changes have occurred in the reproductive system. Whether the
hypothalamus itself is sex differentiated at this early age is not known.
Foetal antlers
437
1 am grateful to Dr Brian Mitchell of the Nature Conservancy for collecting many of the
red deer foetuses used in the study and to Mr Philip Rowe for kindly supplying the testosterone anti-sera used in the testosterone estimations and to Mrs J. Kelly for typing the
manuscript. This work was supported by a grant from the Ford Foundation.
REFERENCES
BURNS, R. K. (1961). In Sex and Internal Secretions, 3rd edn, vol. 1 (ed. W. C. Young),
p. 76. Baltimore: Williams and Wilkins Co.
LINCOLN, G. A. (1971). Puberty in a seasonally breeding male, the red deer stag {Cervus
elaphus L.). /. Reprod. Fert. 25, 41-54.
MANN, T., ROWSON, L. E. A., SHORT, R. V. & SKINNER, J. D. (1967). The relationship
between nutrition and androgenic activity in pubescent twin calves, and the effect of orchitis.
/. Endocr. 38, 455-468.
RETFALVI, L. (1969). Sex dimorphism in foetuses of wapiti, Cervus canadensis. Can. J. Zool.
47, 1418-1419.
WISLOCKI, G. B., AUB, J. C. & WALDO, C. M. (1947). The effect of gonadectomy and the
administration of testosterone proprionate on the growth of antlers in male and female
deer. Endocrinology 40, 202-224.
(Received 26 June 1972, revised 20 August 1972)